With everchanging environmental contexts and dynamic social partners, the ability to continuously integrate information and make adaptations is essential for an animal’s survival and fitness. Early experiences powerfully shape the phenotypic trajectories of offspring, such that conspecifics can exhibit wildly divergent behaviors in the same contexts. The causes and consequences of social behavioral diversity are rooted in the plasticity of neuroendocrine signaling systems, which also serve fundamental roles in the functional and structural development of the brain. Critically, we still know little of the mechanisms by which complex experiences are encoded in the brains of developing offspring to pattern behavioral variation in latter stages of life. This thesis investigates the impact(s) of multifactorial early life experiences on the ontogeny of neural phenotypes in the biparental prairie vole system. In chapter 2, I describe the ages at which distinct subregions of the medial extended amygdala begin to functionally respond to changes in social context. In chapters 3 and 4 I follow with a characterization of how multiple dimensions of the rearing environment independently and synergistically shape the profiles of oxytocin and vasopressin receptors, their peptide-producing cell groups, and age-specific offspring behaviors. The data reveal that region-specific receptor densities are contingent upon an animal’s sex, a father’s presence or absence within the natal nest, the complexity of the juvenile weaning environment, and the higher-order interactions thereof. Furthermore, the absence of a father during the rearing period predicts a more socially permissive offspring phenotype, and lower numbers of oxytocinergic cells in the adult hypothalamus. However, these outcomes are contingent upon family handling conditions, indicating that alternate early life factors can offset or exacerbate the influence of paternal care. Finally, in chapter 5 I describe the reciprocal effect of variation in pup rearing experiences on parental phenotypes. Parental behaviors are surprisingly consistent across parenting contexts, but the associations between behavior and vasopressin cell groups display experience dependent plasticity. Altogether this body of work exhibits the extensive plasticity of behavior and underlying nonapeptide mechanisms, emphasizing the importance of examining environmental interactions within and across the lifespan of the prairie vole.